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Article

How Pseudomonas nitroreducens Passivates Cadmium to Inhibit Plant Uptake

by
Yakui Chen
*,
Yongquan Yu
,
Xiaoyu Fang
,
Yinhuan Zhou
and
Diannan Lu
*
Department of Chemical Engineering, Tsinghua University, Beijing 100084, China
*
Authors to whom correspondence should be addressed.
Appl. Sci. 2024, 14(7), 2857; https://doi.org/10.3390/app14072857
Submission received: 29 February 2024 / Revised: 13 March 2024 / Accepted: 15 March 2024 / Published: 28 March 2024
(This article belongs to the Special Issue Environmental Pollution and Bioremediation Technology)
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Abstract

:
Cadmium (Cd) has been widely used in industry applications, leading to water and soil contamination. This study investigated the potential ability of Pseudomonas nitroreducens (11830) to perform the biosorption of cadmium from aqueous solution and soil. The biosorption characteristics were described using equilibrium isotherm and kinetic studies. The Langmuir adsorption isotherm indicated a better fit with the experimental data (R2 = 0.980), with a maximum capacity of 160.51 mg/g at 30 °C in an initial aqueous solution of 300 mg/L Cd2+. The experiments followed a pseudo-second-order kinetics model (R2 > 0.99), especially at a low initial concentration. The biosorption mechanisms involved were determined through scanning electron microscopy (SEM), transmission electron microscopy (TEM), energy-dispersive spectroscopy (EDS) and protein analysis. The SEM and TEM figures showed that the morphology of cells changed before and after the adsorption of Cd, and the EDS confirmed that Cd was absorbed on the surface of the cell. The analysis of proteins indicated that the protein species increased after the stimulation of Cd, which further confirmed the biosorption mechanism. A pot experiment confirmed that 11830 could passivate the cadmium in soil and reduce its uptake and utilization by Houttuynia cordata Thunb (H. cordata). This work demonstrates the potential application of microorganisms in inhibiting the accumulation of Cd in crops.

1. Introduction

Cadmium (Cd) is a non-essential element of the human body that is carcinogenic [1,2,3,4] and mutagenic. It can cause lung damage and fragile bones [5] and affect calcium regulation in biological systems, and it is one of the most common toxic heavy metals. Even at very low doses, through biomagnification and bioaccumulation [6], cadmium can also pose great harm to humans and the environment [7,8]. With the high speed of developments in industrial operations, large amounts of waste are released into the environment, and free heavy metals cannot be converted into bioavailable forms, resulting in the accumulation of heavy metals in soil and water and the long-term poisoning of the ecological environment on which humans depend [9]. Therefore, research on the presence of cadmium in the environment is useful. A method for controlling heavy metal pollution is necessary, and it is of great significance to protect the soil ecological environment and guarantee the output of agricultural products and food safety.
At present, there are many ways to remove heavy metals, such as electrochemical removal [10,11,12,13,14], chemical precipitation [15,16], ion exchange [17,18] and solvent extraction [19]. However, most of these methods are not suitable for practical application because of their limitations of high cost, high energy requirements, low efficiency, secondary pollution and so on [20]. Compared to the conventional methods mentioned above, the biosorption of heavy metals using environmental microorganisms has become one of the hotspots in the environmental bioremediation field due to the advantages of environmentally friendliness and low operating costs. Biosorption mainly utilizes microbes to reduce the bioavailability of metal ions, thereby inhibiting their accumulation in plants. Bacteria [21,22], fungi [23,24], algae [25,26] and Saccharomyces [9,27,28] are found to be capable of accumulating and removing heavy metals from aqueous solutions and soil, but the underlying mechanism and adsorption properties are not fully understood. The application of the microbial remediation of heavy-metal-contaminated sites is rarely reported.
In this work, bacterium 11830, which was stored in our laboratory, was identified as Pseudomonas nitroreducens through morphological observation, physiological characteristics, 16SrDNA sequencing and phylogenetic tree analysis. Langmuir isotherm, Freundlich isotherm and biosorption kinetics modeling were used for research on the biosorption characteristics of Cd. Then, the SEM, TEM, EDS and protein differential analysis were used to determine the biosorption mechanisms. Finally, the pot test confirmed the ability of strain 11830 to inhibit the adsorption of cadmium by the hyper-enriched plant Houttuynia cordata Thunb (H. cordata), which is of practical application value for reducing the accumulation of cadmium in crops.

2. Materials and Methods

2.1. Cd-Tolerant Strain

Pseudomonas nitroreducens was obtained in our previous study and stored in glycerin tubes at −80 °C, which tolerated Cd of 200 mg/L [29]. Strain 11830 was cultured in Luria–Bertani (LB) medium, which was formulated from 10.0 g peptone (OXOID, LP0042, Hants, UK), 5.0 g yeast extract (OXOID, LP0021, Hants, UK) and 10.0 g sodium chloride (Sinopharm Chemical Reagent Beijing Co., Ltd., 10019318, Beijing, China) per liter at 30 °C pH 7.0 ± 0.2. Cd solutions were prepared by using CdSO4·8/3H2O, Na2HPO4·12H2O and NaH2PO4·2H2O to prepare PBS solutions. The chemicals used in this study were all of analytically pure grade.

2.2. Soil and Houttuynia Cordata

The soil for pot experiments was obtained from Tsinghua campus, and its composition was as follows: 0.89 g/kg of total N, 10.39 g/kg of ammonium N, 24.31 g/kg of nitrate N, 20.29 g/kg of available P and 174.38 g/kg of available K. The soil electric conductivity was 0.55 mS/cm, and the pH was 8.02. A local farmer in the Sichuan Province of China provided the seeds for the Cd-hyperaccumulator H. cordata.

2.3. Identification of Strain

The identification of 11830 was entrusted to Beijing Sanbo Yuanzhi Biotechnology Co., Ltd. (Beijing, China). The 16SrDNA sequence of the bacterium was determined by colony PCR amplification, and the sequence was inputted into the NCBI database BLAST tool for sequence homology analysis and comparison. Then, the molecular evolution tree was constructed by MEGA4 to obtain the known sequence with the highest homology to identify the genus.

2.4. Biosorption

In the current work, 11830 was cultivated in liquid Luria–Bertani medium at 30 °C and 170 rpm by shaking for 3 days. The bacteria were collected by centrifugation at 7000× g for 10 min at 4 °C. After washing with PBS three times and recentrifuging, adding bacteria to different initial concentrations of Cd solution (20, 50, 100, 150, 200, 250 and 300 mg/L) and cultivated in a shake flask with 170 rpm at T = 20, 30 and 40 °C for 24 h. Meanwhile, the cells were added to Cd solutions with different initial concentrations of 20, 50 and 100 mg/L, and Cd concentrations were measured at set intervals by Inductively Coupled Plasma–Atomic Emission Spectrometry (ICP-AES).

2.5. Pot Tests

A pot experiment was conducted to determine the effect of 11830 on Cd uptake by H. cordata. Tsinghua campus soil without heavy metals was air dried at 25 °C and passed through a 100-mesh sieve and set aside. A 1 kg quantity of the experimental soil was mixed with Cd, the treatment concentrations of Cd were 0, 20, 50, 100 and 200 mg/kg soil and each experiment was carried out with 5 replications. After allowing the pot experiments to equilibrate at ambient temperature for a period of seven days, we introduced a 200 mL culture of fresh 11830 cells with an optical density at 600 nm (OD600) of 7.0. This inoculum was thoroughly blended with the soil to ensure uniform distribution. Houttuynia cordata plants, exhibiting 1–2 nascent leaves, were then carefully transplanted into the pots. The cultivation was conducted under controlled conditions at a temperature of 25 ± 2 °C, complemented by natural daylight. The phenological stage of interest, where H. cordata plants reach a leaf count of 3–5, was achieved after approximately 45 days of growth. The plants were harvested and washed with deionized water carefully to remove surface soil and Cd contamination, and then separated into the leaves part and root part. After drying treatment at 70 °C, 0.5 g samples were accurately weighed and digested with a microwave digestion system in order to determine the Cd concentration by Inductively Coupled Plasma–Mass Spectrometry (ICP-MS).

2.6. Statistical Assays

The Cd concentration was analyzed by ICP-AES (IRIS, Thermo Elemental, Waltham, MA, USA) and Inductively Coupled Plasma–Mass Spectrometry (ICP-MS) (ICP QC, Thermo Elemental, Waltham, MA, USA) [30]. All samples were filtered through a 0.22 μm filter membrane prior to testing. The distribution of Cd in 11830 was analyzed by SEM (FEIQuanta 200, FEI Corporation, Hillsboro, OR, USA) and TEM-EDS (H-7650, Hitachi, Tokyo, Japan). Soil and plant samples from potting trials were processed using a microwave digestion system (MARSX, CEM) to obtain cadmium content. The protein composition was analyzed by Mass Spectrometer (Q Exactive, Thermo Scientific, Waltham, MA, USA).
The data were evaluated using ANOVA.

3. Results and Discussions

3.1. Identification of 11830

The 16S rDNA of the 11830 has 99% homology with Pseudomonas nitroreducens, so it was identified as Pseudomonas nitroreducens. The phylogenetic tree of the 11830 is shown in Figure 1.

3.2. Biosorption Isotherms

In order to model biosorption and calculate the biosorption capacity, the Langmuir and Freundlich isotherm models were tested [31,32]. The Langmuir isotherm [33] supposes monolayer sorption is expressed as follows:
Q e = Q m a x b C e 1 + b C e
Qe is the equilibrium sorption amount of Cd (mg/g), Qmax represents the maximum biosorption capacity of 11830 at given temperature (mg/g), Ce is equilibrium concentration of Cd in the solution (mg/L) and b is the biosorption constant.
The Freundlich isotherm [34] is an empirical equation based on the adsorption on heterogeneous surface and is described as follows:
Q e = K C e   1 n
K and n are the biosorption constant.
Biosorption isotherms and biosorption constants evaluated at different temperatures with different initial Cd2+ concentrations are shown in Figure 2 and Table 1. It can be seen that the Langmuir model can describe the biosorption behavior well (R2 > 0.95), which indicated that the adsorption was mainly monolayer biosorption. The maximum biosorption capacity was 160.51 mg/g at 30 °C, and b = 0.004 was higher than that of 20 °C (0.001) and 40 °C (0.001). Higher temperature (40 °C) and low temperature (20 °C) are not conducive to the biosorption process. Near the optimum temperature (30 °C), the lower the temperature is, the more unfavorable to the Cd biosorption. Therefore, the high biosorption capacity of 11830 makes it a promising adsorbent for the removal of Cd, indicating its potential for practical applications in the future.

3.3. Kinetics of the Biosorption Process

It is well known that the adsorption rate is closely related to the initial metal ion concentration [35]. Under low-concentration conditions, the adsorption sites rapidly absorb metal ions and quickly reach equilibrium. However, at higher concentrations, the first stage has the strongest adsorption due to the active site on the surface of the adsorbent [36], and the next stage is equilibrium.
The biosorption kinetics is one of the most important features to describe the biosorption rates [37] and provide the mechanism for the sorption reaction [34]. The experimental data in this study were described by the most popular kinetic models: the Lagergren’s pseudo-first-order [38] as shown in Equation (3) and the pseudo-second-order [39] as shown in Equation (4).
l n ( q e − q t ) = l n q e − k 1 2.303 t
t q t = 1 k 2 q e 2 + t q e
  • qt and qe (mg/g) are the biosorption capacities at time and equilibrium, respectively.
  • t is the reaction time (min).
  • k1 and k2 are the adsorption rate constant of the first- and second-order equation, respectively.
The present experimental biosorption did not follow the pseudo-first-order kinetic, with an R2 for 20, 50 and 100 mg/L of 0.9987, 0.6094 and −0.7128, respectively, so the pseudo-first-order dynamics model diagram is not shown here. However, the pseudo-second-order kinetics provided a good correlation for the biosorption of Cd at all initial concentrations. As shown in Figure 3, qe values were 15.95, 39.95 and 71.48 mg/g with R2 values of 0.9999, 0.9995 and 0.9964 for 20, 50 and 100 mg/L, respectively. The k2 indicated that the biosorption rate of 20 mg/L (k2 = 0.1053) was faster than that of 50 mg/L (k2 = 0.0056) and 100 mg/L (k2 = 0.0012). This result suggests that the biological adsorption process was controlled by chemisorption [40].

3.4. Mechanism of Cd Biosorption on 11830

3.4.1. SEM Analysis

The interaction between microorganisms and heavy metals is the key to carrying out biological repair strategies [41,42]. The cell morphological changes in 11830 before and after Cd adsorption were examined using SEM, as shown in Figure 4. Compared with the original cells (Figure 4a), Pseudomonas nitroreducens 11830 showed different layers of deformation, elongated, and the adsorption of a mass of white particles on the cell surface may have resulted from the adsorption of Cd on the cell surface. It indicated that the presence of Cd can give rise to cell damage. It is speculated that the adsorption mechanism of Cd is mainly the biomineralization of Cd accumulation on the cell surface.

3.4.2. TEM and EDS Analysis

The TEM images are shown in Figure 5a,b. A large amount of high-density electron particles were found on the surface of 11830 after the treatment of Cd2+ (Figure 5b) compared with the original cells (Figure 5a). In order to confirm whether these particles are Cd, elemental analyses of the cell surface were carried out. As shown by the black dots in Figure 5d, EDS spectra were collected and Cd peaks were detected, demonstrating that the absorbed Cd was distributed on the cell surface. This may be attributed to the secretions and surface compositions of 11830 to absorb Cd on the cell surface, or that the self-protecting and detoxifying mechanism removes the intracellular Cd to the cell surface, which can protect cells against high concentrations of Cd [43]. Moreover, these results were also reported by other researchers [44,45].

3.4.3. Protein Differential Analysis

SDS-PAGE was used to qualitatively assess changes in protein expression in 11830 before and after cadmium adsorption. Compared with fresh 11830 cells, the total protein content of 11830 cells was positively regulated after cadmium adsorption, and the variety of proteins increased significantly, which indicated that the cells secreted more proteins to bind to cadmium or to remove cadmium inside the cells to the cell surface to avoid Cd toxicity and further intercepted these bands for mass spectrometer (Q Exactive, Thermo Scientific, Waltham, MA, USA) analysis.
The results showed that the protein content of 11830 increased after the adsorption of cadmium, indicating that the bacterium secreted more proteins because of the stimulation of Cd, which may be due to the production of more functional proteins by the bacterium to bind with Cd ions or to excrete the excess Cd from the intracellular cell to the extracellular cell, so that the bacterium will be protected from the toxicity of Cd. The main differential proteins are shown in Table 2. Most of the new proteins with the functions of adsorbent or resistant heavy metals (such as hydroxylase, dehydrogenase, transaminase, carboxylase, peptidoglycan, periplasmic binding protein, alcohol dehydrogenase zinc-binding domain protein) pump the metal out of the cell (such as catechins iron carrier, ABC transporter family protein, heavy metal efflux pump) [46,47]. This result confirmed the previous speculation that the biosorption of Cd occurred via two mechanisms. One is surface adsorption, in which Cd is adsorbed by the secretions of adsorbents on the cell wall. Another one is the efflux mechanism of the cell, in which Cd is pumped out of the intracellular area, thus being adsorbed on the cell surface. The major protein differences between Cd-treated and Cd-untreated 11830 are listed in the Supporting Information (Tables S1 and S2).

3.5. Pot Tests of 11830 on Biosorption of Cd

H. cordata is a hyperaccumulator of Cd, with high accumulation capacity. In this study, the effect of 11830 on the reduction in Cd bioavailability was investigated using H. cordata as a model plant. The contents of Cd in leaves and roots of the H. cordata are given in Figure 6.
As shown in Figure 6, the Cd content in the leaves part was higher than that in the root part. After inoculation with 11830, the Cd contents in the leaves part and the root part of Houttuynia cordata were 3.087–11.421 mg/kg and 9.062–21.404 mg/kg lower than those in the control group, respectively. At low initial concentrations, both leaves and roots showed no significant differences in the accumulation of Cd in the control groups and treatment groups. When the concentrations of Cd ≥ 50 mg/kg, the accumulation of cadmium in the leaves and roots of the 11830-treated samples was greatly lower than that of the blank samples.
In this study, only small-pot simulation tests were conducted, and if large-scale applications are carried out at a later stage, further field tests must be conducted to obtain reliable data. The ethical and environmental implications of applying live microorganisms in agricultural fields should also be assessed.

3.6. 11830 Passivation Cadmium to Inhibit Adsorption of H. cordata

H. cordata has been demonstrated as a heavy metal hyper-enriched plant [48]. Microorganisms play an important role in enhancing the accumulation of cadmium from soil by H. cordata, and this study has been frequently reported [30,49,50]. But, few studies have been reported on the inhibition of heavy metal uptake by H. cordata or other hyper-enriched plants. Wang et al. [51] reported a composite bacterial agent that produces the phytohormone abscisic acid (ABA). After adsorption, it inhibited the enrichment of Cd in field vegetable crops. The microbial inhibition of cadmium accumulation in cereals was reported by Lou et al. [52]. This result indicated that 11830 is suitable for the biosorption of Cd in soil under conditions of high concentrations, and this adsorbent can inhibit the bioaccumulation of hyper-enriched plants, which has great potential in the bioremediation of cadmium-contaminated soil.
In summary, Figure 7 illustrates that 11830 treatment suppressed the pathway of cadmium enrichment in Houttuynia cordata (arrows indicate the possible path direction of cadmium in plants). 11830 passivated cadmium mainly through extracellular mineralization. In the presence of 11830, cadmium is mainly trapped in the soil by passivation, inhibiting its translocation process in the plant. Under the stimulation of cadmium, the functional proteins, metal transporters and related energy supply systems of 11830 were enhanced to passivate cadmium in the soil from being absorbed and accumulated by H. cordata.

4. Conclusions

In this study, 11830 possessed a good ability for a Cd biosorption capacity of 160.51 mg/g at 30 °C in an initial aqueous solution of 300 mg/L Cd2+. The maximum biosorption capacity of Cd removed by 11830 was 160.51 mg/g at an optical temperature of 30 °C and initial cadmium concentration, and the experiment data were verified to have higher goodness of fit to the Langmuir isotherm than the Freundlich model. The results of kinetic experiments demonstrated that biosorption is rapid, reaching maximum biosorption capacity within a split second and 60 min for low (20 mg/L) and high (>50 mg/L) concentrations of cadmium, respectively. The pseudo-second-order dynamic model has been proved to be applicable to the biosorption of cadmium at any initial concentration, suggesting that the biosorption process was controlled by chemical adsorption. The TEM, EDS and protein studies indicated that both intracellular and extracellular Cd are adsorbed on the surface of the cell, ultimately due to the efflux mechanism and surface adsorption. The results of the pot test showed that 11830 had a good inhibitory effect on the uptake of Cd by H. cordata, and the accumulation of Cd in the leaves and roots of H. cordata was significantly reduced after the soil was treated with 11830. Therefore, the presence of 11830 inhibited the uptake of cadmium by plants and reduced the accumulation of Cd in food. If large-scale applications are carried out at a later stage, further field tests must be conducted to obtain reliable data. The ethical and environmental implications of applying live microorganisms in agricultural fields should also be assessed.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app14072857/s1, Table S1: Protein content before cadmium stimulation. Table S2: Protein content after cadmium stimulation.

Author Contributions

Y.C. and Y.Y. conceived and designed the investigation. Y.C. and Y.Y. conducted the experiments. Y.C. analyzed data and wrote the manuscript. X.F., Y.Z. and D.L. reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by The National Key Research and Development Program of China under Grant number: 2018YFA0902200.

Institutional Review Board Statement

This article does not contain any studies with human participants or animals performed by any authors.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original sequence has been deposited in the NCBI under the GenBank registry number LN995712.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

CdCadmium
SEMScanning electron microscope
TEMTransmission electron microscope
EDSEnergy-dispersive spectroscopy
H. cordataHouttuynia cordata Thunb
TTemperature
ICP-AESInductively Coupled Plasma–Atomic Emission Spectrometry
ICP-MSInductively Coupled Plasma–Mass Spectrometry
PBSPhosphate-buffered saline
PAGEPolyacrylamide gel electrophoresis

References

  1. Hossain, Z.; Huq, F. Studies on the interaction between Cd2+ ions and nucleobases and nucleotides. J. Inorg. Biochem. 2002, 90, 97–105. [Google Scholar] [CrossRef] [PubMed]
  2. Hyder, O.; Chung, M.; Cosgrove, D.; Herman, J.M.; Li, Z.P.; Firoozmand, A.; Gurakar, A.; Koteish, A.; Pawlik, T.M. Cadmium Exposure and Liver Disease among US Adults. J. Gastrointest. Surg. 2013, 17, 1265–1273. [Google Scholar] [CrossRef] [PubMed]
  3. Choi, W.J.; Han, S.H. Blood Cadmium Is Associated with Osteoporosis in Obese Males but Not in Non-Obese Males: The Korea National Health and Nutrition Examination Survey 2008–2011. Int. J. Environ. Res. Public Health 2015, 12, 12144–12157. [Google Scholar] [CrossRef] [PubMed]
  4. Kang, M.Y.; Cho, S.H.; Lim, Y.H.; Seo, J.C.; Hong, Y.C. Effects of environmental cadmium exposure on liver function in adults. Occup. Environ. Med. 2013, 70, 268–273. [Google Scholar] [CrossRef]
  5. Yang, X.F.; Wu, Y.N. Adverse effects of low dose exposures to cadmium below renal damage level should be emphasized for human health effect studies. Zhonghua Yu Fang Yi Xue Za Zhi 2016, 50, 292–295. [Google Scholar] [PubMed]
  6. Xu, C.R.; He, S.B.; Liu, Y.M.; Zhang, W.; Lu, D.N. Bioadsorption and biostabilization of cadmium by Enterobacter cloacae TU. Chemosphere 2017, 173, 622–629. [Google Scholar] [CrossRef] [PubMed]
  7. Zeng, X.X.; Tang, J.X.; Yin, H.Q.; Liu, X.D.; Jiang, P.; Liu, H.W. Isolation, identification and cadmium adsorption of a high cadmium-resistant Paecilomyces lilacinus. Afr. J. Biotechnol. 2010, 9, 6525–6533. [Google Scholar]
  8. Polak-Berecka, M.; Boguta, P.; Ciesla, J.; Bieganowski, A.; Skrzypek, T.; Czernecki, T.; Wasko, A. Studies on the removal of Cd ions by gastrointestinal lactobacilli. Appl. Microbiol. Biotechnol. 2017, 101, 3415–3425. [Google Scholar] [CrossRef] [PubMed]
  9. Marwan, H.; Nassar, D.; Shtaya, M. Heavy metals accumulation in soil and uptake by barley (Hordeum vulgare) irrigated with contaminated water. Sci. Rep. 2023, 13, 4121. [Google Scholar]
  10. Pedersen, K.B.; Jensen, P.E.; Ottosen, L.M.; Lejon, T. An optimised method for electrodialytic removal of heavy metals from harbour sediments. Electrochim. Acta 2015, 173, 432–439. [Google Scholar] [CrossRef]
  11. Pedersen, K.B.; Lejon, T.; Ottosen, L.M.; Jensen, P.E. Screening of variable importance for optimizing electrodialytic remediation of heavy metals from polluted harbour sediments. Environ. Technol. 2015, 36, 2364–2373. [Google Scholar] [CrossRef] [PubMed]
  12. Yoo, J.C.; Yang, J.S.; Jeon, E.K.; Baek, K. Enhanced-electrokinetic extraction of heavy metals from dredged harbor sediment. Environ. Sci. Pollut. Res. 2015, 22, 9912–9921. [Google Scholar] [CrossRef] [PubMed]
  13. Jin, W.; Fu, Y.Q.; Hu, M.Q.; Wang, S.Q.; Liu, Z.G. Highly efficient SnS-decorated Bi2O3 nanosheets for simultaneous electrochemical detection and removal of Cd(II) and Pb(II). J. Electroanal. Chem. 2020, 856, 113744. [Google Scholar] [CrossRef]
  14. Motlochová, M.; Slovák, V.; Pliingrová, E.; Lidin, S.; Subrt, J. Highly-efficient removal of Pb(II), Cu(II) and Cd(II) from water by novel lithium, sodium and potassium titanate reusable microrods. RSC Adv. 2020, 10, 3694–3704. [Google Scholar] [CrossRef] [PubMed]
  15. Mignardi, S.; Corami, A.; Ferrini, V. Evaluation of the effectiveness of phosphate treatment for the remediation of mine waste soils contaminated with Cd, Cu, Pb, and Zn. Chemosphere 2012, 86, 354–360. [Google Scholar] [CrossRef] [PubMed]
  16. Hadasa, K.; Yellaiah, G.; Nagabhushanam, M. Optical and transport properties of Cd0.8Zn0.2S:Cu compounds prepared by modified chemical co-precipitation method. Optik 2014, 125, 6602–6608. [Google Scholar] [CrossRef]
  17. Misra, R.K.; Jain, S.K.; Khatri, P.K. Iminodiacetic acid functionalized cation exchange resin for adsorptive removal of Cr(VI), Cd(II), Ni(II) and Pb(II) from their aqueous solutions. J. Hazard. Mater. 2011, 185, 1508–1512. [Google Scholar] [CrossRef] [PubMed]
  18. Koiodynska, D.; Krukowska-Bak, J.; Kazmierczak-Razna, J.; Pietrzak, R. Uptake of heavy metal ions from aqueous solutions by sorbents obtained from the spent ion exchange resins. Microporous Mesoporous Mater. 2017, 244, 127–136. [Google Scholar] [CrossRef]
  19. Selatnia, A.; Boukazoula, A.; Kechid, N.; Bakhti, M.Z.; Chergui, A. Biosorption of Fe3+ from aqueous solution by a bacterial dead Streptomyces rimosus biomass. Process Biochem. 2004, 39, 1643–1651. [Google Scholar] [CrossRef]
  20. Mack, C.; Wilhelmi, B.; Duncan, J.R.; Burgess, J.E. Biosorption of precious metals. Biotechnol. Adv. 2007, 25, 264–271. [Google Scholar] [CrossRef]
  21. Banerjee, G.; Pandey, S.; Ray, A.K.; Kumar, R. Bioremediation of Heavy Metals by a Novel Bacterial Strain Enterobacter cloacae and Its Antioxidant Enzyme Activity, Flocculant Production, and Protein Expression in Presence of Lead, Cadmium, and Nickel. Water Air Soil Pollut. 2015, 226, 91. [Google Scholar] [CrossRef]
  22. Pan, X.H.; Wu, W.; Lu, J.; Chen, Z.; Li, L.; Rao, W.H.; Guan, X. Biosorption and extraction of europium by Bacillus thuringiensis strain. Inorg. Chem. Commun. 2017, 75, 21–24. [Google Scholar] [CrossRef]
  23. Yan, C.; Viraraghavan, T. Mechanism of biosorption of heavy metals by Mucor rouxii. Eng. Life Sci. 2008, 8, 363–371. [Google Scholar] [CrossRef]
  24. Yang, S.Q.; Sun, X.X.; Shen, Y.P.; Chang, C.; Guo, E.H.; La, G.X.; Zhao, Y.; Li, X.Z. Tolerance and Removal Mechanisms of Heavy Metals by Fungus Pleurotus ostreatus HAAS. Water Air Soil Pollut. 2017, 228, 130. [Google Scholar] [CrossRef]
  25. Cheng, J.F.; Yin, W.K.; Chang, Z.Y.; Lundholm, N.; Jiang, Z.M. Biosorption capacity and kinetics of cadmium(II) on live and dead Chlorella vulgaris. J. Appl. Phycol. 2017, 29, 211–221. [Google Scholar] [CrossRef]
  26. Edris, G.; Alhamed, Y.; Alzahrani, A. Biosorption of Cadmium and Lead from Aqueous Solutions by Chlorella vulgaris Biomass: Equilibrium and Kinetic Study. Arab. J. Sci. Eng. 2014, 39, 87–93. [Google Scholar] [CrossRef]
  27. Vasudevan, P.; Padmavathy, V.; Dhingra, S.C. Kinetics of biosorption of cadmium on Baker’s yeast. Bioresour. Technol. 2003, 89, 281–287. [Google Scholar] [CrossRef] [PubMed]
  28. Goksungur, Y.; Uren, S.; Guvenc, U. Biosorption of cadmium and lead ions by ethanol treated waste baker’s yeast biomass. Bioresour. Technol. 2005, 96, 103–109. [Google Scholar] [CrossRef] [PubMed]
  29. Yu, Y.Q.; Huang, W.W.; Dong, J.J.; Zhu, Q.F.; Lu, D.N.; Liu, Y.M. Study on the Removal of Cd(II) by Pseudomonas nitroreducens: Biosorption Characteristics and Mechanism. China Environ. Sci. 2017, 37, 7. [Google Scholar]
  30. Chen, Y.K.; Zhu, Q.F.; Dong, X.Z.; Huang, W.W.; Du, C.Y.; Lu, D.N. How Serratia marcescens HB-4 absorbs cadmium and its implication on phytoremediation. Ecotoxicol. Environ. Saf. 2019, 185, 109723. [Google Scholar] [CrossRef]
  31. Argun, M.E.; Dursun, S.; Ozdemir, C.; Karatas, M. Heavy metal adsorption by modified oak sawdust: Thermodynamics and kinetics. J. Hazard. Mater. 2007, 141, 77–85. [Google Scholar] [CrossRef] [PubMed]
  32. Hameed, B.H.; Ahmad, A.A.; Aziz, N. Isotherms, kinetics and thermodynamics of acid dye adsorption on activated palm ash. Chem. Eng. J. 2007, 133, 195–203. [Google Scholar] [CrossRef]
  33. Langmuir, I. The Adsorption of Gases on Plane Surfaces of Glass, Mica and Platinum. J. Am. Chem. Soc. 1918, 40, 1361–1403. [Google Scholar] [CrossRef]
  34. Freundlich, H. Concerning adsorption in solutions. Z. Fur Phys. Chem.-Stochiom. Verwandtschaftslehre 1906, 57, 385–470. [Google Scholar]
  35. Joo, J.H.; Hassan, S.H.A.; Oh, S.E. Comparative study of biosorption of Zn2+ by Pseudomonas aeruginosa and Bacillus cereus. Int. Biodeterior. Biodegrad. 2010, 64, 734–741. [Google Scholar] [CrossRef]
  36. Wierzba, S. Biosorption of nickel (II) and zinc (II) from aqueous solutions by the biomass of yeast Yarrowia lipolytica. Pol. J. Chem. Technol. 2017, 19, 1–10. [Google Scholar] [CrossRef]
  37. Huang, F.; Dang, Z.; Guo, C.L.; Lu, G.N.; Gu, R.R.; Liu, H.J.; Zhang, H. Biosorption of Cd(II) by live and dead cells of Bacillus cereus RC-1 isolated from cadmium-contaminated soil. Colloids Surf. B Biointerfaces 2013, 107, 11–18. [Google Scholar] [CrossRef] [PubMed]
  38. Njikam, E.; Schiewer, S. Optimization and kinetic modeling of cadmium desorption from citrus peels: A process for biosorbent regeneration. J. Hazard. Mater. 2012, 213–214, 242–248. [Google Scholar] [CrossRef] [PubMed]
  39. Ho, Y.S.; McKay, G. Pseudo-second order model for sorption processes. Process Biochem. 1999, 34, 451–465. [Google Scholar] [CrossRef]
  40. Li, Y.; Dai, Y.; Tao, Q.Q.; Gao, Z.; Xu, L. Ultrahigh efficient and selective adsorption of U(VI) with amino acids-modified magnetic chitosan biosorbents: Performance and mechanism. Int. J. Biol. Macromol. 2022, 214, 54–66. [Google Scholar] [CrossRef]
  41. Park, J.H.; Lamb, D.; Paneerselvam, P.; Choppala, G.; Bolan, N.; Chung, J.W. Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. J. Hazard. Mater. 2011, 185, 549–574. [Google Scholar] [CrossRef] [PubMed]
  42. Chibuike, G.U.; Obiora, S.C. Heavy metal polluted soils: Effect on plants and bioremediation methods. Appl. Environ. Soil Sci. 2014, 2014, 752708. [Google Scholar] [CrossRef]
  43. Pabst, M.W.; Miller, C.D.; Dimkpa, C.O.; Anderson, A.J.; McLean, J.E. Defining the surface adsorption and internalization of copper and cadmium in a soil bacterium, Pseudomonas putida. Chemosphere 2010, 81, 904–910. [Google Scholar] [CrossRef]
  44. Lin, Y.B.; Wang, X.Y.; Wang, B.P.; Mohamad, O.; Wei, G.H. Bioaccumulation characterization of zinc and cadmium by Streptomyces zinciresistens, a novel actinomycete. Ecotoxicol. Environ. Saf. 2012, 77, 7–17. [Google Scholar] [CrossRef]
  45. Hambuckersberhin, F.; Remacle, J. Cadmium Sequestration in Cells of 2 Strains of Alcaligenes-Eutrophus. FEMS Microbiol. Ecol. 1990, 73, 309–315. [Google Scholar] [CrossRef]
  46. Uraguchi, S.; Kamiya, T.; Clemens, S.; Fujiwara, T. Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiol. Plant. 2014, 151, 339–347. [Google Scholar] [CrossRef]
  47. Chang, N.; Yao, S.Y.; Chen, D.G.; Zhang, L.L. Research progress on the mechanisms of cadmium transport. Chem. Life 2018, 38, 483–490. [Google Scholar]
  48. Kayser, A.; Wenger, K.; Keller, A.; Attinger, W.; Felix, H.R.; Gupta, S.K.; Schulin, R. Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous Soil: The use of NTA and sulfur amendments. Environ. Sci. Technol. 2000, 34, 1778–1783. [Google Scholar] [CrossRef]
  49. Zhou, L.; Chen, W.; Hou, L. Notice of Retraction: The Cadmium Accumulation Ability of Huttuynia cordata Enhanced by Microorganisms in Soil. In Proceedings of the 5th International Conference on Bioinformatics and Biomedical Engineering, Wuhan, China, 10–12 May 2011; pp. 1–6. [Google Scholar]
  50. Wang, L.; Lin, H.; Dong, Y.B.; He, Y.H. Effects of cropping patterns of four plants on the phytoremediation of vanadium-containing synthetic wastewater. Ecol. Eng. 2018, 115, 27–34. [Google Scholar] [CrossRef]
  51. Wang, H.; Wang, S.T.; He, X.L.; Xie, M.H.; Cai, M.Z.; Zhu, Y.X.; Du, S.T. A promising product: Abscisic acid-producing bacterial agents for restricting cadmium enrichment in field vegetable crops. Food Chem. X 2023, 19, 100795. [Google Scholar] [CrossRef]
  52. Lou, F.; Fu, T.L.; He, G.D.; Tian, W.J.; Wen, J.C.; Yang, M.F.; Wei, X.L.; He, Y.; He, T.B. Different composites inhibit Cd accumulation in grains under the rice-oilseed rape rotation mode of karst area: A field study. Ecotoxicol. Environ. Saf. 2023, 256, 114884. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Phylogenetic tree of 11830 based on 16SrDNA gene.
Figure 1. Phylogenetic tree of 11830 based on 16SrDNA gene.
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Figure 2. Langmuir and Freundlich plots of Cd biosorption by strain.
Figure 2. Langmuir and Freundlich plots of Cd biosorption by strain.
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Figure 3. Pseudo-second-order kinetic plots of Cd biosorption by 11830 at initial 20, 50 and 100 mg/L concentrations.
Figure 3. Pseudo-second-order kinetic plots of Cd biosorption by 11830 at initial 20, 50 and 100 mg/L concentrations.
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Figure 4. SEM images before (a) and after (b) treatment with 200 mg/L Cd2+.
Figure 4. SEM images before (a) and after (b) treatment with 200 mg/L Cd2+.
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Figure 5. TEM plots and EDS spectra before and after adsorption of Cd: (a) control of TEM; (b) Cd-loaded cells of TEM; (c) control of EDS; (d) Cd-loaded cells of EDS; Cd2+: 200 mg/L.
Figure 5. TEM plots and EDS spectra before and after adsorption of Cd: (a) control of TEM; (b) Cd-loaded cells of TEM; (c) control of EDS; (d) Cd-loaded cells of EDS; Cd2+: 200 mg/L.
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Figure 6. Uptake of Cd by H. cordata after bioremediation by 11830.
Figure 6. Uptake of Cd by H. cordata after bioremediation by 11830.
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Figure 7. The possible mechanism of 11830 inhibition Cd uptake by Houttuynia cordata: (a) not treated with 11830; (b) treatment with 11830.
Figure 7. The possible mechanism of 11830 inhibition Cd uptake by Houttuynia cordata: (a) not treated with 11830; (b) treatment with 11830.
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Table 1. Isothermal adsorption equation and related parameters.
Table 1. Isothermal adsorption equation and related parameters.
T (°C)Langmuir ModelFreundlich Model
Qmax (mg/g)bR2nKR2
20118.320.0010.9801.1880.2350.981
30160.510.0040.9771.5032.0120.949
40127.860.0010.9591.1810.3210.946
Table 2. Differential protein before and after stimulation with Cd.
Table 2. Differential protein before and after stimulation with Cd.
MW [KDa]DescriptionAmino Acid Sequence
Coverage
BlankExperiment
9.3Interferon-induced transmembrane protein016.3
15.1Acyl-CoA thioesterase017.42
15.5Blue light-and temperature-regulated antirepressor YcgF06.94
15.7Lipocalin07.41
15.9Aerotaxis sensor receptor protein011.27
16.7CAMP-binding protein05.1
17.1Exclusion suppressor07.74
18.618 k peptidoglycan-associated outer membrane lipoprotein047.67
22.4Aerotaxis receptor05.57
23.62-octaprenyl-3-methyl-6-methoxy-1,4-benzoquinol hydroxylase06.91
24.5Glutaminyl-tRNA synthetase04.78
27.9Zinc import ATP-binding protein ZnuC09.96
28.2Zn-dependent protease with chaperone function023.51
29.3Bacterial transcriptional regulator family protein05.22
31.63,4-dihydroxyphenylacetate 2,3-dioxygenase05.32
38.123S rRNA (guanosine-2′-O-)-methyltransferase RlmB06.38
39.5Metallo-beta-lactamase family protein04.46
42.8C4-type zinc finger protein019.32
42.92-octaprenyl-6-methoxyphenyl hydroxylase05.72
44.8Outer membrane efflux protein032.13
47.9Trigger factor031.32
49.22,4-diaminobutyrate 4-transaminase015.22
61.0Bacterial leucyl aminopeptidase010.37
62.9Arsenic ABC transporter ATPase04.08
64.0Bacterial extracellular solute-binding family protein012.65
67.3BipA GTPase014.5
72.8Metal-transporting P-type ATPase transmembrane protein01.42
79.6Zinc-regulated outer membrane050.75
82.5Catecholate siderophore receptor Fiu017.18
88.0Aerobic respiration control sensor protein01.54
116.3Heavy metal efflux pump, cobalt-zinc-cadmium04.39
175.9Alpha-2-macroglobulin025.71
18.8Adenosylcobinamide kinase10.980
33.62-nitropropane dioxygenase17.30
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Chen, Y.; Yu, Y.; Fang, X.; Zhou, Y.; Lu, D. How Pseudomonas nitroreducens Passivates Cadmium to Inhibit Plant Uptake. Appl. Sci. 2024, 14, 2857. https://doi.org/10.3390/app14072857

AMA Style

Chen Y, Yu Y, Fang X, Zhou Y, Lu D. How Pseudomonas nitroreducens Passivates Cadmium to Inhibit Plant Uptake. Applied Sciences. 2024; 14(7):2857. https://doi.org/10.3390/app14072857

Chicago/Turabian Style

Chen, Yakui, Yongquan Yu, Xiaoyu Fang, Yinhuan Zhou, and Diannan Lu. 2024. "How Pseudomonas nitroreducens Passivates Cadmium to Inhibit Plant Uptake" Applied Sciences 14, no. 7: 2857. https://doi.org/10.3390/app14072857

APA Style

Chen, Y., Yu, Y., Fang, X., Zhou, Y., & Lu, D. (2024). How Pseudomonas nitroreducens Passivates Cadmium to Inhibit Plant Uptake. Applied Sciences, 14(7), 2857. https://doi.org/10.3390/app14072857

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